Skip to main content
Log in

Diversity of Oil-Degrading Microorganisms in the Gulf of Finland (Baltic Sea) in Spring and in Summer

  • Experimental Articles
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Diversity of the oil-degrading microbial strains isolated from the water and sediments of the Gulf of Finland (Baltic Sea) in winter and in summer was studied. Substrate specificity of the isolates for aliphatic and aromatic hydrocarbons was studied. The isolates belonged to 32 genera of the types Proteobacteria (alpha-, beta-, and gammaproteobacteria), Actinobacteria,Firmicutes, and Bacteroidetes. Seasonal variations of the oil-degrading microbial communities was revealed. The presence of the known genes responsible for the degradation of oil aliphatic and aromatic hydrocarbons was determined. The alkB sequence of the alkane hydroxylase gene was found in ~16% of the studied strains. The sequence of the phnAc phenanthrene 3,4- dioxygenase was found in Sphingobacterium sp. and Arthrobacter sp. isolates retrieved in winter and summer. In five Pseudomonas sp. strains from winter samples, the classical operons of naphthalene degradation (nah) were localized in catabolic plasmids, of which three belonged to IncР-9, one, to IncР-7, and two to an unidentified incompatibility group. Burkholderia and Delftia strains contained the operons for naphthalene degradation via salicylate and gentisate (nag). The presence of nag genes has not been previously reported for Delftia spp. strains. The sequences of the nagG salicylate 5-hydroxylase gene were also found in Achromobacter, Sphingobacterium, and Stenotrophomonas strains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bakirov, E.A., Ermolkin, V.I., Larin, V.I., Mal’tsev, A.K., and Rozhkov, E.L., Geologiya nefti i gaza (Oil and Gas Geology), Moscow: Nedra, 1990.

    Google Scholar 

  • De Bruyne, K., Slabbinck, B., Waegeman, W., Vauterin, P., De Baets, B., and Vandamme, P., Bacterial species identification from MALDI-TOF mass spectra through data analysis and machine learning, Syst. Appl. Microbiol., 2011, vol. 34, pp. 20–29.

    Article  PubMed  Google Scholar 

  • Evans, W.C., Fernley, H.N., and Griffiths, E., Oxidative metabolism of phenantrene and anthracene by soil pseudomonads: the ring-fission mechanism, J. Biochem., 1965, vol. 95, pp. 819–831.

    Article  CAS  Google Scholar 

  • Ferrero, M., Llobet-Brossa, E., Lalucat, J., Garcia-Valdes, E., Rosselo-Mora, R., and Bosch, R., Coexistence of two distinct copies of naphthalene degradation genes in Pseudomonas strains isolated from the western mediterranean region, Appl. Environ. Microbiol., 2002, vol. 68, pp. 957–962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greated, A. and Thomas, C.M. A pair of PCR primers for IncP-9 plasmids, Microbiology (UK), 1999, vol. 145, pp. 3003–3004.

    Article  Google Scholar 

  • Griffin, R., Churchill, P., Churchill, S., and Jones, L., Biodegradation rate enhancement of hydrocarbons by an oleophilic fertilizer and a rhamnolipid biosurfactant, J. Environ. Qual., 1995, vol. 24, pp. 19–28.

    Google Scholar 

  • HELCOM, HELCOM Annual Report on Discharges Observed during Aerial Surveillance in the Baltic Sea, 2015, 2016.

    Google Scholar 

  • Izmalkova, T.Y., Sazonova, O.I., Nagornih, M.O., Sokolov, S.L., Kosheleva, I.A., and Boronin, A.M., The organization of naphthalene degradation genes in Pseudomonas putida strain AK5, Res. Microbiol., 2013, vol. 164, pp. 244–253.

    Article  CAS  PubMed  Google Scholar 

  • Izmalkova, T.Yu., Mavrodi, D.V., Sokolov, S.L., Kosheleva, I.A., and Boronin, A.M., Molecular classification of IncP-9 naphthalene degradation plasmids, Plasmid, 2006, vol. 56, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  • Izmalkova, T.Yu., Sazonova, O.I., Kosheleva, I.A., and Boronin, A.M., Phylogenetic analysis of the genes for naphthalene and phenanthrene degradation in Burkholderia sp. strains, Russ. J. Genet., 2013, vol. 49, no. 6, pp. 609–616.

    Article  CAS  Google Scholar 

  • Izmalkova, T.Yu., Sazonova, O.I., Sokolov, S.L., Kosheleva, I.A., and Boronin, A.M., The P-7 incompatibility group plasmids responsible for biodegradation of naphthalene and salicylate in fluorescent pseudomonads, Microbiology (Moscow), 2005, vol. 74, no. 3, pp. 290–295.

    Article  CAS  Google Scholar 

  • Jutkina, J., Heinaru, E., Vedler, E., Juhanson, J., and Heinaru, A., Occurrence of plasmids in the aromatic degrading bacterioplankton of the Baltic Sea, Genes, 2011, vol. 2, pp. 853–868.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimura, M., The Neutral Theory of Molecular Evolution, Cambridge University Press, Cambridge, 1983.

    Book  Google Scholar 

  • Kostka, J.E., Prakash, O., Overholt, W.A., Green, S.J., Freyer, G., Canion, A., Delgardio, J., Norton, N., Hazen, T.C., and Huettel, M., Hydrocarbondegrading bacteria and the bacterial community response in gulf of Mexico beach sands impacted by the deepwater horizon oil spill, Appl. Environ. Microbiol., 2011, vol. 77, pp. 7962–7974.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreitsberg, R., Tuvikene, A., Barsiene, J., Fricke, N.F., Rybakovas, A., Andreikenaite, L., Rumvolt, K., and Vilbaste, S., Biomarkers of environmental contaminants in the coastal waters of Estonia (Baltic Sea): effects on eelpouts (Zoarces viviparus), J. Environ. Monit., 2012, vol. 14, pp. 2298–2308.

    Article  CAS  PubMed  Google Scholar 

  • Laurie, A.D. and Lloyd-Jones, G., Quanification of phnAc and nahAc in contaminated New Zealand soils by competitive PCR, Appl. Environ. Microbiol., 2000, vol. 66, pp. 1814–1817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurie, A.D. and Lloyd-Jones, G., The phn genes of Burkholderia sp. strain RP007 constitute a divergent gene cluster for polycyclic aromatic hydrocarbon catabolism, J. Bacteriol. 1999, vol. 181, pp. 531–540.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peix, A., Ramirez-Bahena, M.-H., and Velazquez, E., Historical evolution and current status of the taxonomy of genus Pseudomonas, Infect. Genet. Evol., 2009, vol. 9, pp. 1132–1147.

    Article  PubMed  Google Scholar 

  • Reunamo, A., Riemann, L., Leskinen, P., and Jørgensen, K.S., Dominant petroleum hydrocarbondegrading bacteria in the Archipelago Sea in South-West Finland (Baltic Sea) belong to different taxonomic groups than hydrocarbon degraders in the oceans, Mar. Pollut. Bull., 2013, vol. 72, pp. 174–180.

    Article  CAS  PubMed  Google Scholar 

  • Riemann, L., Leitet, C., Pommier, T., Simu, K., Holmfeldt, K., Larsson, U., and Hagström, Å., The native bacterioplankton community in the central Baltic Sea is influenced by freshwater bacterial species, Appl. Environ. Microbiol., 2008, vol. 74, pp. 503–515.

    Article  CAS  PubMed  Google Scholar 

  • Rojo, F., Degradation of alkanes by bacteria, Environ. Microbiol., 2009, vol. 11, pp. 2477–2490.

    Article  CAS  PubMed  Google Scholar 

  • Rossello-Mora, R.A., Lalucat, J., and Garcia-Valdes, E., Comparative biochemical and genetic analysis of naphthalene degradation among Pseudomonas stutzeri strain, Appl. Environ. Microbiol., 1994, vol. 60, pp. 966–972.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 1989.

    Google Scholar 

  • Sokolov, S.L., Sazonova, O.I., Gafarov, A.B., Ivanova, A.A., Vetrova, A.A., Prisiazhnaya, N.V., Kosheleva, I.A., and Boronin, A.M., Assessment of degradative potential of oil-oxidizing microorganisms of the Baltic Sea in model microcosms, Biotechnology in Russia, 2017, vol. 33, no. 4, pp. 76–84.

    Google Scholar 

  • Timmis, K.N., Lehrbach, P.R., Harayama, S., Don, R.H., Mermod, N., Bas, S., Leppick, R., Weightman, A.J., Reineke, W., and Knackmuss, H.-J., Analysis and manipulation of plasmid-encoded pathways for the catabolism of aromatic compounds by soil bacteria, in Plasmids in Bacteria, Helinski, D.R., Cohen, C.N., Clewell, D.B., Jackson, D.A., and Hollaender, A., Eds., N.-Y.: Plenum, 1985, pp. 719–739.

    Chapter  Google Scholar 

  • Van Beilen, J.B. and Funhoff, E.G., Alkane hydroxylases involved in microbial alkane degradation, Appl. Microbiol. Biotechnol., 2007, vol. 74, pp. 13–21.

    Article  CAS  PubMed  Google Scholar 

  • Van de Peer, Y. and De Wachter, R., TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment, Comput. Applic. Biosci., 1994, vol. 10, pp. 569–570.

    Google Scholar 

  • Viggor, S., Juhanson, J., Jõesaar, M., Mitt, M., Truu, J., Vedler, E., and Heinaru, A., Dynamic changes in the structure of microbial communities in the Baltic Sea coastal seawater microcosms modified by crude oil, shale oil or diesel fuel, Microbiol. Res., 2013, vol. 168, pp. 415–427.

    Article  CAS  PubMed  Google Scholar 

  • Wilkstrom, P., Wilklund, A., Anderson, A.C., and Forman, M., DNA recovery and PCR quantification of catechol-2,3-dioxygenase genes from different soil types, J. Biotechnol., 1996, vol. 52, pp. 107–120.

    Article  Google Scholar 

  • Yakimov, M.M., Timmis, K.N., and Golyshin, P.N., Obligate oil-degrading marine bacteria, Curr. Opin. Biotechnol., 2007, vol. 18, pp. 257–266.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Y.Y., Wang, J., Liao, J.Q., Xie, S.G., and Huang, Y., Abundance and diversity of soil petroleum hydrocarbondegrading microbial communities in oil exploring areas, Appl. Microbiol. Biotechnol., 2015, vol. 99, pp. 1935–1946.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, N.Y., Fuenmayor, S.L., and Williams, P.A., nag genes of Ralstonia (formerly Pseudomonas) sp. strain U2 encoding enzymes for gentisate catabolism, J. Bacteriol., 2001, vol. 183, pp. 700–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Yu. Izmalkova.

Additional information

Original Russian Text © T.Yu. Izmalkova, A.B. Gafarov, O.I. Sazonova, S.L. Sokolov, I.A. Kosheleva, A.M. Boronin, 2018, published in Mikrobiologiya, 2018, Vol. 87, No. 2, pp. 204–216.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Izmalkova, T.Y., Gafarov, A.B., Sazonova, O.I. et al. Diversity of Oil-Degrading Microorganisms in the Gulf of Finland (Baltic Sea) in Spring and in Summer. Microbiology 87, 261–271 (2018). https://doi.org/10.1134/S0026261718020054

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261718020054

Keywords

Navigation